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 Table of Contents  
Year : 2020  |  Volume : 32  |  Issue : 2  |  Page : 119-126

Relationship of bone mineral density with panoramic radiomorphometric indices in tobacco users in India

1 Department of Oral Medicine and Radiology, Government Dental College and Research Institute, Bengaluru, Karnataka, India
2 Department of Oral Medicine and Radiology, PGIDS, Rohtak, Haryana, India

Date of Submission11-Apr-2020
Date of Decision21-May-2020
Date of Acceptance23-May-2020
Date of Web Publication27-Jun-2020

Correspondence Address:
Dr. Anju Redhu
Senior Lecturer, Department of Oral Medicine and Radiology, PGIDS, Rohtak- 124 001, Haryana
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jiaomr.jiaomr_57_20

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Background: Osteoporosis is a crippling disease that can eventually culminate in fracture. Smoking and smokeless tobacco (SLT) use are important contributors to this disease. Decreased bone mineral density (BMD) which marks osteoporotic bone changes are assessed using dual energy X-ray absorptiometry (DXA). Panoramic radiomorphometric indices (RI) which are inexpensive and widely used in dentistry also provide architectural details of jawbones. Hence the study was attempted to find the relationship between BMD and panoramic RI in tobacco users in the Indian Population. Materials and Methods: The hundred subjects were divided into study groups comprising 25 smokers, 25 SLT users, 25 subjects with a combination of habits, and 25 healthy controls were subjected to BMD assessment using DXA scan and digital panoramic radiographs for calculation of mandibular cortical index (MCI), mental index (MI), and panoramic mandibular index (PMI). Results: SLT users had the least values of BMD (P <0.05). Both MI and PMI were markedly reduced in SLT users and had a strong positive correlation to BMD (r=0.600, P- value -0.002 for MI and r= 0.428, P value -0.033 for PMI). A strong negative correlation of MCI to BMD (rs= -0.510, P- value 0.009), MI (rs= -0.632, P- value-0.001),and PMI (rs= -0.432, P- value 0.031) was noted in SLT users with a maximum number of C3 found among them. However, no significant correlation of BMD with RI was obtained in smokers. The practise of both smoking and SLT showed a significant positive correlation of BMD to MI and PMI. Conclusion: Tobacco was found to have detrimental effects on BMD, well reflected in RI of MCI, MI, and PMI, thus, oral physicians must screen and educate tobacco users, particularly, SLT users for impaired bone health and refer them promptly for suitable treatment.

Keywords: Bone density, osteoporosis, panoramic, radiography, smoking, smokeless tobacco

How to cite this article:
Suman B, Redhu A. Relationship of bone mineral density with panoramic radiomorphometric indices in tobacco users in India. J Indian Acad Oral Med Radiol 2020;32:119-26

How to cite this URL:
Suman B, Redhu A. Relationship of bone mineral density with panoramic radiomorphometric indices in tobacco users in India. J Indian Acad Oral Med Radiol [serial online] 2020 [cited 2020 Sep 19];32:119-26. Available from: http://www.jiaomr.in/text.asp?2020/32/2/119/288140

   Introduction Top

In India according to Global Adult Tobacco Survey (GATS) conducted by CDC (Centers for Disease Control and Prevention) and WHO (World Health Organisation) in 2016–17, 28.6% adults (42.4% males and 14.2% females) are tobacco users.[1] Tobacco products contain over 7,000 potentially toxic constituents, which can cause various morbid diseases like certain types of cancer, cardiovascular disease, respiratory ailments, and bone diseases like osteoporosis.[2]

Osteoporosis, the most common bone disease, is a growing public health concern entailing a significant socioeconomic impact. In the United States, it is projected three million fractures occur annually because of osteoporosis, with an estimated economic cost of $25.3 billion by 2025.[2] India is reported to bear the burden of over 50 million people with low bone mass or osteoporotic bone alterations.[3] Since most of osteoporotic individuals remain asymptomatic for a long duration, utmost attention is required for their screening, to institute prevention, early diagnosis, and prompt treatment.

Risk factors for osteoporosis include both smoking and smokeless forms of tobacco, which are found to be harmful to bone health through multiple mechanisms. Few studies have shown that smoking does not affect bone mass.[3],[4],[5]

World Health Organization has identified low bone mineral density (BMD) measurements to show osteoporosis and fracture risk.[6] Although dual-energy X-ray absorptiometry (DXA) is accepted as the gold standard method of BMD assessment, and is routinely performed at three skeletal sites—the lumbar spine, proximal femur, and distal forearm, where it is expressed as a T-score; it is costly and not widely available.[7] Panoramic radiographs provide a suitable alternative to DXA, in that they are simple, non-invasive, quick, and economical.[8] Various studies have elaborated on the role of panoramic radiomorphometric indices(RI), measured on digital panoramic radiographs(PRs), in identifying low BMD and the risk for osteoporosis.[9] Mandibular BMD is significantly correlated with that of the hip, forearm, and lumbar vertebral BMD.[10]

Effects of tobacco in its smoking [2] and smokeless forms [11] on the skeletal system were extensively studied but no studies in the literature have attempted to correlate the BMD of the tobacco users with the panoramic RI of the mandible. It can be hypothesized that tobacco use affects the normal bone turnover mechanism which results in lower BMD, and could be assessed on the panoramic radiographs by the use of RI. Panoramic radiographs which are widely used in dentistry as screening tools, and can, aid oral clinicians to detect low BMD in tobacco users which could cause better management, resulting in a decreased socioeconomic impact of osteoporosis. To the best of our knowledge, no study has been done till now which attempts to highlight the usefulness of panoramic radiographs in establishing the deleterious effects of tobacco on bone using RI.

With the above-stated aim, this study was taken up to assess the mandibular cortical bone changes among tobacco users using RI (MCI, MI, PMI), and to relate the findings with their BMD, assessed using DXA of the distal forearm.

   Material and Methods Top

Patients included in this study were from the outpatient department of Oral Medicine and Radiology. This cross-sectional study was conducted on 100 subjects aged above 25 years who consented voluntarily to be part of the study.

Included patients were categorized as study group (tobacco users), comprising 25 smokers (as per definition),[12] 25 Smokeless Tobacco users (SLT) (as per definition),[13] and 25 individuals with a combination of smoking and smokeless tobacco habits; control group comprised of 25 healthy age and sex- matched individuals with no habit of tobacco use. Panoramic radiographs of the included patients who visited the Department of Oral Medicine and Radiology for complaints related to odontogenic causes were taken.

Patients with a history of systemic disease, chemoradiotherapy, drugs affecting bone health, pathological jaw lesions, edentulous lower jaw, and fracture of jaw/wrist (in the non-dominant arm), were excluded.

DXA scan (using Lunar Prodigy Advance DXA System, analysis version 13.60, GE Healthcare) of the distal part of the radius bone in the non-dominant arm was performed for all included patients. T scores, Z scores, and BMD (in gm/cm 2) were recorded. Distal radius was selected because it is rich in cortical bone, more responsive to age- related changes,[14] require comparatively less radiation exposure, and recently proposed to be more representative of osteoporosis than central sites (spine and lumbar).[15] Previous studies had provided a significant relation between mandibular radiomorphometric indices and BMD of the distal radius.[10]

All digital panoramic radiographs were taken by a single operator using 9000 Digital Panoramic and Cephalometric system, (Carestream, France) at 70 kVp; 10 mA, 14.3s with standard head position and were viewed on a flat panel monitor under subdued lighting, and analyzed at a resolution of 322 dpi by two observers, who were calibrated beforehand and blinded to the results of DXA. Measurements were performed using MicroDicom- free DICOM viewer 0.9.1(build 918) 32- bit software.

Radiomorphometric indices were determined using the measuring tool of the in-built computer software program:

  1. Mandibular cortical index (MCI) was determined by the visual appearance of the lower border of the mandible below the mental foramen on both sides of the panoramic radiographs and categorized into one of three groups according to the classification by Klemetti et al.,1994 which is: C1, the endosteal margin of the cortex is even and sharp on both sides; C2, the endosteal margin shows semilunar defects (lacunar resorption) and/or seems to form endosteal cortical residues on one or both sides; C3, the cortical layer forms heavy endosteal cortical residues and is porous [Figure 1]a, [Figure 1]b.[16]
  2. Mental index (MI) was determined by tracing a line perpendicular to a tangent drawn to the lower border of mandible through the centre of the mental foramen. The cortical width was measured at this point (Ledgerton et al.- 1999) [Figure 2].[17]
  3. Panoramic mandibular index (PMI) as proposed by Benson et al. in 1991 was assessed as the ratio between cortical thickness at the base of the mandible, and the distance from the center of the mental foramen to the lower border of base of the mandible [Figure 3].[17]
Figure 1: Evaluation of mandibular cortex -(a) MCI-C2. (b) MCI-C3

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Figure 2: MI (Mental Index) evaluation

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Figure 3: PMI (Panoramic Mandibular Index) evaluation

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To overcome the bias of memory, two measurements were taken bilaterally in the mandible at an interval of 1 month by both observers and the average was reported for MI and PMI. The data so obtained were correlated with the BMD values of the subjects.

The charted data was analyzed using SPSS V.17.0. Descriptive data statistics, cross-tabulations, and Chi-square statistics were computed. Intra and interobserver agreement were calculated using Cronbach's alpha(α). One-way ANOVA with posthoc Scheffe test was used for multiple comparisons of mean values between groups. The level of statistical significance was determined at P value<0.05. Pearson correlation for parametric variables and Spearman correlations for non-parametric variables (MCI) were applied.

   Results Top

The present study comprising of 75 tobacco users and 25 healthy controls (70 males and 30 females). Their ages ranged from 25 to 74 years (mean age 42.93 ±13.85 years)[Graph 1]. All the smokers and combination habit group subjects were men while the SLT users group comprised of 17females (68%) and eight males (32%).

The study demonstrated marked Intra and inter-observer agreement with Cronbach's alpha value (α)>0.96 (a single value has been provided to assess the overall agreement). Details are provided in [Table 1].
Table 1: Intra-observer andInter-observer Crohnbach's alpha values of the two observers-

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Although no statistically significant difference was noted among the study subgroups for the mean values of MI and PMI, the mean MI was least for SLT users (3.84mm±1.260) and highest for smokers (4.46mm± 0.725) whereas PMI was least for controls (0.303± 0.104) and maximum for smokers (0.318± 0.070) [Table 2].
Table 2: Distribution of age, frequency and duration of habit, MI, PMI and BMD among the study subjects and controls

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A fairly equal number of SLT users(n=16) and combination group(n=17) subjects demonstrated C2 category MCI. An equal number of smokers (n=12) had MCI category C1 and C2. Controls also showed category C2 (n=12) more than C1 and C3. TheC3 type of mandibular cortical morphology was most numerous in SLT users (n=4) than other groups [Graph 2].

The highest mean BMD value of 0.907± 0.064 g/cm 2 was present in smokers and SLT users had the least BMD value of 0.730± 0.155 g/cm 2;(P- value-0.000) [Table 2].

The frequency of tobacco use/day in the study group was divided as 1–5, 6–10, 11–15, 16–20, and >20 times/day. Mean frequency was 8.25 ± 5.17 per day with maximum frequency noted among the combination habit group (10.56±5.62), followed by SLT users (7.52±5.54) and smokers (6.68±4.36). Smokers having a frequency of 11–15 clouds of smoke/day had the least PMI value of 0.258(P<0.05). SLT users with a frequency of 16–20 chews/day had the least BMD of 0.466g/cm 2 (P<0.05).

Duration of tobacco use among the study groups was categorized as 1–5, >5–10, >10–15, >15–20, >20–25, and >25 years with a mean of 12.10 ± 7.58 years. SLT users had the longest duration of habit (15.16±10.20) followed by a combination habit group (10.60±6.73) and smokers (10.56±5.80) [Table 2]. The duration of habit did not yield any statistically significant association with PMI, MI, and BMD values in smokers and in combination habit groups. However, the SLT group gave a statistically significant association of BMD with a duration of practice of habit, with the least mean BMD score of 0.515g/ cm 2, noted in subjects, habituated for >25 years (P≤ 0.05).

As per World Health Organization criteria, patients can be classified as normal (T-score ≥-1.0 standard deviation), osteopenic (T score,-1.0 to -2.5 standard deviation), and osteoporotic (T-score≤-2.5 standard deviation).[9] Accordingly, majority of the tobacco users (52%, n=39) had osteopenia (smokers- 11, SLT group-11 and combination group- 17) and 16% (n=12) had osteoporotic scores (smokers - 1, SLT group-8 and combination group- 3). Among controls, normal bone health prevailed among 52% (n=13), while 40% (n=10) had osteopenia and 8% (n=2) had osteoporotic scores [Table 3].
Table 3: Distribution of bone health among the study subjects and controls

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There was a strong negative correlation between age and BMD values. The age group of 31–40 years possessed the highest mean BMD value (0.879±0.106).A statistically significant difference was noted when BMD of SLT users was compared with that of control group (P- value-0.006), smokers (P- value -0.000), and combination habit group (P- value -0.002).

A cut off value of <3mm for MI and a ratio of ≤0.25 for PMI was considered for referral of patients for further investigation for osteoporosis.[18] MI attributed a statistically significant association with bone health among controls (P- value -0.000), SLT users (P- value -0.033), and patients with combined habits (P- value -0.022). 32% (n=8) of the SLT users were osteoporotic, among whom 4 patients were having MI ≤ 3.0mm. All smokers had MI ≥3mm. No statistically significant association of study groups was obtained with the threshold value of PMI, however, it was significant for the control group. MCI and bone health showed a statistically significant association (P value<0.05) in SLT users and smokers. All the patients with MCI category C3 were osteoporotic [Table 4]. The Sensitivity and specificity obtained for the MI were 50.0% and 97.3%, respectively.PMI yielded a sensitivity and specificity of 42.8% and 91.8%, respectively. To assess sensitivity and specificity of MCI, C1 was considered as normal and C2 and C3 were considered as eroded forms.[19] The sensitivity and specificity for the MCI Index was 78.5% and 47.6%, respectively.
Table 4: Association of bone health with threshold values of MI, PMI and MCI among the study group and control group

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In the present study, the controls demonstrated a strong positive correlation of BMD to panoramic RI (r=0.610, P- value -0.001 with MI; r= 0.460, P value -0.021 with PMI). In smokers, no significant correlation was noted among BMD and age (r = -0.188, P- value -0.368), MI (r=-0.224, P- value -0.283), and PMI (r = -0.124, P- value -0.555). In SLT users, BMD was negatively correlated to age (r=-0.661, P value -0.000).A significant positive correlation of BMD was noted with MI (r= 0.600, P value -0.002) and PMI (r= 0.428, P- value -0.033) [Table 5]. MCI showed a strong negative correlation to BMD (rs= -0.510, P- value -0.009), MI (rs= -0.632, P- value -0.001), and PMI (rs= -0.432, P- value -0.031)[Table 6].
Table 5: Pearson Correlation (r) of different variables among the study groups and control group

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Table 6: Spearman Correlation (rs) of MCI and other variables among the study groups and control group

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The duration of habit had a strong negative correlation with MI, PMI, and BMD. In combination habit group, BMD values showed significant positive correlation to both MI (r= 0.396, P value -0.050) and PMI (r= 0.461, P value -0.020)[Table 5].

   Discussion Top

Tobacco affects bone remodeling by decreasing the circulating levels of vitamin D, possibly via enhanced hepatic metabolism of vitamin D metabolites. It increases oxidative stress, decreases serum parathormone (PTH) level, and inhibits its action on Ca 2+ reabsorption in renal tubules, impairing bone health.[2] Its use is associated with decreased levels of estrogen and testosterone, resulting in decreased bone mineral density.[20] SLT products inhibit osteoblastic metabolism, and may contain areca nut, which gets locally absorbed and affects viability and gene expressions of alkaline phosphatase, receptor activator of nuclear factor Kappa-β ligand(RANKL) and osteoprotegerin.[11] This promotes osteoclast-mediated bone resorption. SLT has nicotine, which induces vasoconstriction, low tissue oxygen tension, and tissue ischemia, thus adversely affecting bone health.[21] The pathophysiological mechanisms of tobacco in causing decreased BMD and increased fracture risk are concise and depicted in [Figure 4].
Figure 4: Patho-physiological mechanism of tobacco for causing decreased BMD and increased fracture risk

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These effects of tobacco cumulatively affect the skeletal system, including the mandible sensitive to changes in body bone mass.[22] This is reflected as increased cortical porosity and thinning which can be assessed using Panoramic RI. To the best of our knowledge, this is the first study to explore a relationship between the panoramic RI and BMD in tobacco users.

The present study revealed a low BMD score in the smokeless tobacco users group, compared to to other groups and controls. 32% (n=8) subjects were found to have osteoporosis in the SLT group, as compared to 8% (n=2) in the control group. These findings are following the findings of Abbas et al. (2015),[11] Quandt et al. (2006)[21], and Bakan et al. 2013.[23] The BMD scores showed a progressive decrease with an increase in the habit's duration. Besides, the typical single dose of nicotine from chewing tobacco is 15 times that of cigarettes. With such high concentrations of nicotine, SLT not only decreases bone oxygen consumption and collagen synthesis but also causes increased levels of inflammatory mediators locally that can promote alveolar bone loss.[24]

Generally, most of the scientific literature links cigarette smoking as a risk factor for osteoporosis and its associated risk of fractures. However, some studies have shown that smoking does not affect bone density.[4],[5] Possible explanations for these differences include variations in bone sites examined and methods of bone density measurement, endpoints of interest, age, and menopausal status of subjects; and source of subjects.[25]

In this study cigarette smoking was not found to be associated with BMD loss, a finding akin to the findings of Moinuddin et al.,[26] who reported a negative effect of smoking only on low birth weight individuals, but contrasting to the findings of many studies that associate smoking with lower bone mass.[5],[27] In the present study, a relatively lower mean age and duration of habit (mean duration-10.56 years) among the smokers might have contributed to higher BMD scores compared to other sub-groups. All the smokers were males, who have a lower tendency to lose bone than women.[5]

The present study reported a reduced mean BMD among patients with combination habits, reaffirming the findings of Yusuf et al. (2014)[28] who reported that, as compared to never tobacco users, only the ever use of both snuff and cigarette smoking in the past or currently was significantly associated with osteoporosis. Combined use increases the cumulative levels of nicotine in blood and thus has increased adverse effects. In the present study, mean MI and PMI values were least (3.84mm; 0.305±0.104)in SLT users. Also, the C3 category predominated in them than the other groups. The duration of SLT use showed a strong negative correlation to the indices and BMD marking its detrimental effects on bone. In SLT users, both MI and PMI had a strong positive correlation to BMD. Previous studies conducted by researchers also reported that the findings of BMD can be reflected in the RI.[6],[9] A strong negative correlation of MCI to MI, PMI, and BMD was noted in SLT users reaffirming the role of smokeless tobacco in contributing to increased porosity of mandibular inferior cortex.

No significant correlation was noted between BMD and PMI, MI, in smokers probably owing to the lesser duration of habit and the lower mean age of the smokers in this study. The combination of smoking and SLT use might adjunctively affect bone as a statistically significant positive correlation was noted between BMD, MI, and PMI in the combination habit group.

Previous studies reported that mandibular cortical width below 3 mm at the mental foramen region may be considered as threshold value when predicting low spinal and femoral BMD (osteoporosis or osteopenia) and is a criterion for referring patients for densitometric evaluation.[9],[18] In this study, 5 SLT users had MI < 3mm (P<0.05). Sensitivity for MI in detecting osteoporosis in present study was 50.0%, which is comparatively less as reported by the literature (ranges from 60.2 to 88.5%).[9],[19],[29] However, the present study reported a high specificity (97.3%) for MI which is congruent to the findings of Muramatsu et al., who also reported same specificity.[9] Other studies reported relatively less specificity (54.1-78.5%).[9],[19],[29] PMI yielded a sensitivity of 42.8% and specificity of 91.8%. Literature has reported a relatively higher sensitivity (ranges between 71.7 and 85%) but lower specificity (58–80%) as compared to the present study.[9],[19],[30] The difference could be attributed to the threshold value considered and highlight the role of MI and PMI in the screening of osteoporosis.

For determination of sensitivity and specificity of MCI, C2 and C3 groups were considered as one group.[19] Sensitivity for the MCI Index was 78.5% which is more as reported by previous studies.[9],[19] Gaur et al. reported a 100% sensitivity to MCI.[6] The present study reported comparatively less specificity of 47.6% as compared to the previous studies (range is 75–96%).[6],[9],[19] Thus, MCI could be a diagnostic tool for low BMD levels in tobacco users and for their referral to the specialists.

The limitations of this study were that the study sample size was small. Wide age range, the menopausal status of female subjects, body weight, physical activity level, nutritional status, dietary, and lifestyle factors might have affected the values obtained. Also, it remains to be further ascertained if these indices carry practical utility in dental clinics of general dental practitioners who may need additional and adequate training to use the panoramic indices effectively on their patients.



Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Ethical consideration

The ethical clearance was taken from the institutional ethical committee (Reference letter No.GDCRI/ACM(2)/5/2017-18).

Financial support and sponsorship


Conflicts of interest

There are no conflicts of interest.

   References Top

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  [Figure 1], [Figure 2], [Figure 3], [Figure 4]

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5], [Table 6]


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